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The involvement of nuclear domains and proteins in plant responses to virus infections

The interactions between a virus and its host cell play a central role in the viral infection cycle. The analysis of virus-host interactions is critical for understanding the mechanisms of viral infections and for the development of novel antiviral strategies.

Viruses are obligate intracellular pathogens with small genomes and, therefore, are reliant on subverting the cellular functions and machineries to facilitate their own replication.

The cell nucleus is one of the key features of eukaryotic cells. It is a highly dynamic, membrane-bound organelle that hosts major cellular events, including DNA replication, messenger RNA synthesis and processing, and ribosome subunit biogenesis.

Given the pivotal role of the nucleus in cell host function, it is not surprising that viruses interact with this organelle and its compartments, and that such interactions play a crucial role in the virus infection cycle. The nucleolus and Cajal bodies (CBs) are prominent sub-nuclear domains involved in a number of critical processes within the nucleus. Certain viruses interact with these compartments but the functions of such interactions are largely uncharacterised.

We have recently shown that the ability of the umbravirus ORF3 protein to move viral RNA long distances through the phloem strictly depends on its interaction with CBs, the nucleolus and the nucleolar protein, fibrillarin. The ORF3 protein targets and re-organizes CBs and then enters the nucleolus by causing fusion of these structures with the nucleolus. This process is mediated by the interaction between the ORF3 protein and a major nucleolar protein, fibrillarin.

We provide a model whereby the ORF3 protein utilises trafficking pathways between CBs and the nucleolus, and recruits fibrillarin for the formation of viral cytoplasmic ribonucleoprotein particles capable of long-distance movement and systemic infection.

We have found that some other viruses also have interactions with the nucleolus and CBs. For example, our recent results demonstrate that CBs are involved in the plant defence response (resistance) against tobraviruses (Tobacco rattle virus) and hordeiviruses (barley stripe mosaic virus) but that disruption of CBs interferes with the infection cycle of potyviruses (Potato virus Y and Plum pox virus).

More detailed analysis has demonstrated that nucleolar translocation of the CB signature protein, coilin, can mediate antiviral defence. Indeed, the nucleolar-targeted 16K protein of the plant virus, tobacco rattle virus (TRV) elicits the hypersensitive response (HR), a type of plant programmed cell death (PCD) in wild-type tobacco plants as demonstrated by necrosis and other hallmarks of PCD. In our studies to elucidate the mechanism of the TRV 16K–mediated HR, we have demonstrated that the 16K protein interacts with coilin, the major scaffolding protein of CBs and partially re-distributes it to the nucleolus. Invasion of the nucleolus by the 16K-coilin complex leads to induction of signalling pathways underpinning the PCD-based HR. The HR serves to prevent the spread of the virus from the infection site thereby providing an antivirus defence mechanism. These results demonstrate novel functions for coilin as an essential component of the host antiviral defence and may have implications for other plant and animal viruses that interact with the nucleolus and CBs. Our preliminary results also suggest a role of both fibrillarin and coilin in the signal transduction mechanisms in response to environmental cues.

Another example of a virus that utilises with the nucleolus is PMTV. Investigating the interactions between plant viruses and the nucleolus and CBs will facilitate the design of novel strategies to control plant virus infections. In addition, other recent results demonstrate that the nucleolus and CBs are also involved in responses to abiotic stresses, perhaps allowing the plant to monitor environmental changes. 


Areas of Interest

Printed from /research/groups/cell-and-molecular-sciences/virus-research/host-pathogen-interactions/nucleolar-biology on 26/04/18 12:34:57 PM

The James Hutton Research Institute is the result of the merger in April 2011 of MLURI and SCRI. This merger formed a new powerhouse for research into food, land use, and climate change.